Escherichia coli strain Nissle 1917 ameliorates experimental colitis by modulating intestinal permeability, the inflammatory response and clinical signs in a faecal transplantation model

Journal of Medical Microbiology

Volumn 65, Issue 3, 2016, Pages 201-210

  Souza, Éricka L ^a   Elian, Samir D ^a   Paula, Laís M ^a   Garcia, Cristiana C ^b   Vieira, Angélica T ^a   Teixeira, Mauro M ^a   Arantes, Rosa M ^a   Nicoli, Jacques R ^a   Martins, Flaviano S ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; PROBIOTIC AGENT; DEXTRAN SULFATE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; COLITIS; CONTROLLED STUDY; EOSINOPHIL COUNT; ESCHERICHIA COLI; EVALUATION STUDY; FECAL MICROBIOTA TRANSPLANTATION; FEMALE; HISTOPATHOLOGY; IMMUNE RESPONSE; INTESTINE MUCOSA PERMEABILITY; LYMPHOCYTE COUNT; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TREATMENT OUTCOME; ANIMAL; BAGG ALBINO MOUSE; CHEMICALLY INDUCED; CLASSIFICATION; FECES; GERMFREE ANIMAL; INFLAMMATION; INTESTINE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PERMEABILITY; PHYSIOLOGY;

ANIMALS; COLITIS; DEXTRAN SULFATE; ESCHERICHIA COLI; FECES; FEMALE; GERM-FREE LIFE; INFLAMMATION; INTESTINES; MICE; MICE, INBRED BALB C; PERMEABILITY; PROBIOTICS;

EID: 84960810691     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.000222     Document Type: Article

References (66)

1. Abraham, C. & Medzhitov, R. (2011). Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology 140, 1729–1737.
2. Adar, T., Shteingart, S., Ben Ya’acov, A., Bar-Gil Shitrit, A. & Goldin, E. (2014). From airway inflammation to inflammatory bowel disease: eotaxin-1, a key regulator of intestinal inflammation. Clin Immunol 153, 199–208.
3. Al-Haddad, S. & Riddell, R. H. (2005). The role of eosinophils in inflammatory bowel disease. Gut 54, 1674–1675.
4. Albert, E. J., Duplisea, J., Dawicki, W., Haidl, I. D. & Marshall, J. S. (2011). Tissue eosinophilia in a mouse model of colitis is highly dependent on TLR2 and independent of mast cells. Am J Pathol 178, 150–160.
5. Atarashi, K., Tanoue, T., Oshima, K., Suda, W., Nagano, Y., Nishikawa, H., Fukuda, S., Saito, T., Narushima, S. & other authors (2013). Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500, 232–236.
6. Baumgart, D. C. & Sandborn, W. J. (2007). Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet 369, 1641–1657.
7. Bibiloni, R., Fedorak, R. N., Tannock, G. W., Madsen, K. L., Gionchetti, P., Campieri, M., De Simone, C. & Sartor, R. B. (2005). VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100, 1539–1546.
8. Blumberg, R. S. (2009). Inflammatory bowel disease: immunologic considerations. In Current Diagnosis & Treatment in Gastroenterology, Hepatology and Endoscopy, pp. 11–21. Edited by N. J. Greenberger, R. S. Blumberg & R. Burakoff. New York: McGraw-Hill Medical.
9. Cerf-Bensussan, N. & Gaboriau-Routhiau, V. (2010). The immune system and the gut microbiota: friends or foes? Nat Rev Immunol 10, 735–744.
10. Chassaing, B., Koren, O., Goodrich, J. K., Poole, A. C., Srinivasan, S., Ley, R. E. & Gewirtz, A. T. (2015). Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519, 92–96.
11. COBEA (2006). Colégio Brasileiro de Experimentação Animal. Legislação e Ética. Available from: http://www.cobea.org.br/. Accessed 30 June, 2011.
12. Cui, H. H., Chen, C. L., Wang, J. D., Yang, Y. J., Cun, Y., Wu, J. B., Liu, Y. H., Dan, H. L., Jian, Y. T. & Chen, X. Q. (2004). Effects of probiotic on intestinal mucosa of patients with ulcerative colitis. World J Gastroenterol 10, 1521–1525.
13. Dongarrá, M. L., Rizzello, V., Muccio, L., Fries, W., Cascio, A., Bonaccorsi, I. & Ferlazzo, G. (2013). Mucosal immunology and probiotics. Curr Allergy Asthma Rep 13, 19–26.
14. Elian, S. D., Souza, E. L., Vieira, A. T., Teixeira, M. M., Arantes, R. M., Nicoli, J. R. & Martins, F. S. (2015). Bifidobacterium longum subsp. infantis BB-02 attenuates acute murine experimental model of inflammatory bowel disease. Benef Microbes 6, 277–286.
15. FAO/WHO Report (2002). Guidelines for the Evaluation of Probiotics in Food, London/Ontario: Food and Agricultural Organization/ World Health Organization Working Group.
16. Fedorak, R. N. & Madsen, K. L. (2004). Probiotics and the management of inflammatory bowel disease. Inflamm Bowel Dis 10, 286–299.
17. Furusawa, Y., Obata, Y., Fukuda, S., Endo, T. A., Nakato, G., Takahashi, D., Nakanishi, Y., Uetake, C., Kato, K. & other authors (2013). Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504, 446–450.
18. Geem, D., Harusato, A., Flannigan, K. & Denning, T. L. (2015). Harnessing regulatory T cells for the treatment of inflammatory bowel disease. Inflamm Bowel Dis 21, 1409–1418.
19. Ghouri, Y. A., Richards, D. M., Rahimi, E. F., Krill, J. T., Jelinek, K. A. & DuPont, A. W. (2014). Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease. Clin Exp Gastroenterol 7, 473–487.
20. Grant, C. R., Liberal, R., Mieli-Vergani, G., Vergani, D. & Longhi, M. S. (2015). Regulatory T-cells in autoimmune diseases: challenges, controversies and yet–unanswered questions. Autoimmun Rev 14, 105–116.
21. Himmel, M. E., Hardenberg, G., Piccirillo, C. A., Steiner, T. S. & Levings, M. K. (2008). The role of T-regulatory cells and Toll-like receptors in the pathogenesis of human inflammatory bowel disease. Immunology 125, 145–153.
22. Huttenhower, C., Kostic, A. D. & Xavier, R. J. (2014). Inflammatory bowel disease as a model for translating the microbiome. Immunity 40, 843–854.
23. Johnson-Henry, K. C., Donato, K. A., Shen-Tu, G., Gordanpour, M. & Sherman, P. M. (2008). Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157: H7-induced changes in epithelial barrier function. Infect Immun 76, 1340–1348.
24. Kaser, A., Zeissig, S. & Blumberg, R. S. (2010). Inflammatory bowel disease. Annu Rev Immunol 28, 573–621.
25. Kelly, D. & Mulder, I. E. (2012). Microbiome and immunological interactions. Nutr Rev 70 (Suppl 1), S18–S30.
26. Klingberg, T. D., Pedersen, M. H., Cencic, A. & Budde, B. B. (2005). Application of measurements of transepithelial electrical resistance of intestinal epithelial cell monolayers to evaluate probiotic activity. Appl Environ Microbiol 71, 7528–7530.
27. Kobayashi, Y. (2008). The role of chemokines in neutrophil biology. Front Biosci 13, 2400–2407.
28. Kruger, P., Saffarzadeh, M., Weber, A. N. R., Rieber, N., Radsak, M., von Bernuth, H., Benarafa, C., Roos, D., Skokowa, J. & Hartl, D. (2015). Neutrophils: between host defence, immune modulation, and tissue injury. PLoS Pathog 11, e1004651.
29. Kruis, W., Frič, P., Pokrotnieks, J., Luká s, M., Fixa, B., Kascá k, M., Kamm, M. A., Weismueller, J., Beglinger, C. & other authors (2004). Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53, 1617–1623.
30. Lepage, P., Häsler, R., Spehlmann, M. E., Rehman, A., Zvirbliene, A., Begun, A., Ott, S., Kupcinskas, L., Doré, J. & other authors (2011). Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology 141, 227–236.
31. Loftus, E. V. Jr. & Sandborn, W. J. (2002). Epidemiology of inflammatory bowel disease. Gastroenterol Clin North Am 31, 1–20.
32. Logan, I. & Bowlus, C. L. (2010). The geoepidemiology of autoimmune intestinal diseases. Autoimmun Rev 9, A372–A378.
33. Maloy, K. J. & Powrie, F. (2011). Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474, 298–306.
34. Manichanh, C., Borruel, N., Casellas, F. & Guarner, F. (2012). The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol 9, 599–608.
35. Martins, F. S., Elian, S. D., Vieira, A. T., Tiago, F. C., Martins, A. K., Silva, F. C., Souza, E. L. S., Sousa, L. P., Araújo, H. R. & other authors (2011). Oral treatment with Saccharomyces cerevisiae strain UFMG 905 modulates immune responses and interferes with signal pathways involved in the activation of inflammation in a murine model of typhoid fever. Int J Med Microbiol 301, 359–364.
36. Martins, F. S., Vieira, A. T., Elian, S. D., Arantes, R. M., Tiago, F. C., Sousa, L. P., Araújo, H. R., Pimenta, P. F., Bonjardim, C. A. & other authors (2013). Inhibition of tissue inflammation and bacterial translocation as one of the protective mechanisms of Saccharomyces boulardii against Salmonella infection in mice. Microbes Infect 15, 270–279.
37. Molodecky, N. A., Soon, I. S., Rabi, D. M., Ghali, W. A., Ferris, M., Chernoff, G., Benchimol, E. I., Panaccione, R., Ghosh, S. & other authors (2012). Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142, 46–54, e42, quiz e30.
38. Neuman, M. G. (2007). Immune dysfunction in inflammatory bowel disease. Translational Research 149, 173–186.
39. Neurath, M. F. (2014). Cytokines in inflammatory bowel disease. Nat Rev Immunol 14, 329–342.
40. Ordás, I., Eckmann, L., Talamini, M., Baumgart, D. C. & Sandborn, W. J. (2012). Ulcerative colitis. Lancet 380, 1606–1619.
41. Orel, R. & Kamhi Trop, T. (2014). Intestinal microbiota, probiotics and prebiotics in inflammatory bowel disease. World J Gastroenterol 20, 11505–11524.
42. Perše, M. & Cerar, A. (2012). Dextran sodium sulphate colitis mouse model: traps and tricks. J Biomed Biotechnol 2012, 1–13.
43. Powrie, F., Leach, M. W., Mauze, S., Caddie, L. B. & Coffman, R. L. (1993). Phenotypically distinct subsets of CD4+T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol 5, 1461–1471.
44. Raphael, I., Nalawade, S., Eagar, T. N. & Forsthuber, T. G. (2015). T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine 74, 5–17.
45. Rigottier-Gois, L. (2013). Dysbiosis in inflammatory bowel diseases: the oxygen hypothesis. ISME J 7, 1256–1261.
46. Rogler, G. (2011). Prebiotics and probiotics in ulcerative colitis: where do we stand? Digestion 84, 126–127.
47. Rudensky, A. Y. (2011). Regulatory T cells and Foxp3. Immunol Rev 241, 260–268.
48. Satokari, R. (2015). Contentious host-microbiota relationship in inflammatory bowel disease – can foes become friends again? Scand J Gastroenterol 50, 34–42.
49. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671–675.
50. Schultz, M., Strauch, U. G., Linde, H. J., Watzl, S., Obermeier, F., Göttl, C., Dunger, N., Grunwald, N., Schölmerich, J. & Rath, H. C. (2004). Preventive effects of Escherichia coli strain Nissle 1917 on acute and chronic intestinal inflammation in two different murine models of colitis. Clin Diagn Lab Immunol 11, 372–378.
51. Sha, S., Xu, B., Kong, X., Wei, N., Liu, J. & Wu, K. (2014). Preventive effects of Escherichia coli strain Nissle 1917 with different courses and different doses on intestinal inflammation in murine model of colitis. Inflamm Res 63, 873–883.
52. Smith, P. M., Howitt, M. R., Panikov, N., Michaud, M., Gallini, C. A., Bohlooly, Y. M., Glickman, J. N. & Garrett, W. S. (2013). The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341, 569–573.
53. Strath, M., Warren, D. J. & Sanderson, C. J. (1985). Detection of eosinophils using an eosinophil peroxidase assay. Its use as an assay for eosinophil differentiation factors. J Immunol Methods 83, 209–215.
54. Talley, N. J., Abreu, M. T., Achkar, J. P., Bernstein, C. N., Dubinsky, M. C., Hanauer, S. B., Kane, S. V., Sandborn, W. J., Ullman, T. A. & other authors (2011). An evidence-based systematic review on medical therapies for inflammatory bowel disease. Am J Gastroenterol 106 (Suppl 1), S2–S25, quiz S26.
55. Tiago, F. C., Porto, B. A., Ribeiro, N. S., Moreira, L. M., Arantes, R. M., Vieira, A. T., Teixeira, M. M., Generoso, S. V., Nascimento, V. N. & other authors (2015). Effect of Saccharomyces cerevisiae strain UFMG A-905 in experimental model of inflammatory bowel disease. Benef Microbes 6, 807–815.
56. Travers, J. & Rothenberg, M. E. (2015). Eosinophils in mucosal immune responses. Mucosal Immunol 8, 464–475.
57. Triantafillidis, J. K., Merikas, E. & Georgopoulos, F. (2011). Current and emerging drugs for the treatment of inflammatory bowel disease. Drug Des Devel Ther 5, 185–210.
58. Valatas, V., Bamias, G. & Kolios, G. (2015). Experimental colitis models: insights into the pathogenesis of inflammatory bowel disease and translational issues. Eur J Pharmacol 759, 253–264.
59. Venturi, A., Gionchetti, P., Rizzello, F., Johansson, R., Zucconi, E., Brigidi, P., Matteuzzi, D. & Campieri, M. (1999). Impact on the composition of the faecal flora by a new probiotic preparation: preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment Pharmacol Ther 13, 1103–1108.
60. Vieira, A. T., Pinho, V., Lepsch, L. B., Scavone, C., Ribeiro, I. M., Tomassini, T., Ribeiro-dos-Santos, R., Soares, M. B., Teixeira, M. M. & Souza, D. G. (2005). Mechanisms of the anti-inflammatory effects of the natural secosteroids physalins in a model of intestinal ischaemia and reperfusion injury. Br J Pharmacol 146, 244–251.
61. Vieira, A. T., Fagundes, C. T., Alessandri, A. L., Castor, M. G., Guabiraba, R., Borges, V. O., Silveira, K. D., Vieira, E. L., Gonçalves, J. L. & other authors (2009). Treatment with a novel chemokine-binding protein or eosinophil lineage-ablation protects mice from experimental colitis. Am J Pathol 175, 2382–2391.
62. Vieira, A. T., Teixeira, M. M. & Martins, F. S. (2013). The role of probiotics and prebiotics in inducing gut immunity. Front Immunol 4, 1–12.
63. Wang, L., Ray, A., Jiang, X., Wang, J. Y., Basu, S., Liu, X., Qian, T., He, R., Dittel, B. N. & Chu, Y. (2015). T regulatory cells and B cells cooperate to form a regulatory loop that maintains gut homeostasis and suppresses dextran sulfate sodium-induced colitis. Mucosal Immunol 8, 1297–1312.
64. Woodruff, S. A., Masterson, J. C., Fillon, S., Robinson, Z. D. & Furuta, G. T. (2011). Role of eosinophils in inflammatory bowel and gastrointestinal diseases. J Pediatr Gastroenterol Nutr 52, 650–661.
65. Yan, Y., Kolachala, V., Dalmasso, G., Nguyen, H., Laroui, H., Sitaraman, S. V. & Merlin, D. (2009). Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS One 4, e6073.
66. Zocco, M. A., dal Verme, L. Z., Cremonini, F., Piscaglia, A. C., Nista, E. C., Candelli, M., Novi, M., Rigante, D., Cazzato, I. A. & other authors (2006). Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 23, 1567–1574.